Human epidermal growth factor receptor (HER1) aligned on the plasma membrane adopts key features of Drosophila EGFR asymmetry

Biochemical Society Transactions

Volumn 40, Issue 1, 2012, Pages 184-188

  Martin Fernandez, Marisa L ^a  

^a Science and Technology Facilities Council   (United Kingdom)

Author keywords

Epidermal growth factor receptor (EGFR); Fluorescence lifetime imaging microscopy (FLIM); F rster resonance energy transfer (FRET); Human epidermal growth factor receptor (HER1); Receptor tyrosine kinase (RTK)

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; TYROSINE KINASE RECEPTOR;

BINDING AFFINITY; CELL HETEROGENEITY; CELL MEMBRANE; CRYSTAL STRUCTURE; DROSOPHILA; EPITHELIUM CELL; HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; DROSOPHILA PROTEINS; EPIDERMAL GROWTH FACTOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; SIGNAL TRANSDUCTION;

INVERTEBRATA;

EID: 84856268766     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110692     Document Type: Review

References (39)

1. Schlessinger, J. (2000) Cell signaling by receptor tyrosine kinases. Cell 103, 211-225
2. Yarden, Y. and Sliwkowski, M.X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137 (Pubitemid 33674041)
3. Downward, J., Parker, P. and Waterfield, M.D. (1984) Autophosphorylation sites on the epidermal growth-factor receptor. Nature 311, 483-485 (Pubitemid 14035459)
4. Paez, J.G., Janne, P.A., Lee, J.C., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F.J., Lindeman, N., Boggon, T.J. et al. (2004) EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy. Science 304, 1497-1500 (Pubitemid 38720929)
5. Jackman, D.M., Miller, V.A., Cioffredi, L.A., Yeap, B.Y., Janne, P.A., Riely, G.J., Ruiz, M.G., Giaccone, G., Sequist, L.V. and Johnson, B.E. (2009) Impact of epidermal growth factor receptor and KRAS mutations on clinical outcomes in previously untreated non-small cell lung cancer patients: results of an online tumor registry of clinical trials. Clin. Cancer Res. 15, 5267-5273
6. Ullrich, A., Coussens, L., Hayflick, J.S., Dull, T.J., Gray, A., Tam, A.W., Lee, J., Yarden, Y., Libermann, T.A., Schlessinger, J. et al. (1984) Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309, 418-425 (Pubitemid 14102443)
7. Zhang, X.W., Gureasko, J., Shen, K., Cole, P.A. and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149 (Pubitemid 43866200)
8. Brewer, M.R., Choi, S.H., Alvarado, D., Moravcevic, K., Pozzi, A., Lemmon, M.A. and Carpenter, G. (2009) The juxtamembrane region of the EGF receptor functions as an activation domain. Mol. Cell 34, 641-651
9. Jura, N., Endres, N.F., Engel, K., Deindl, S., Das, R., Lamers, M.H., Wemmer, D.E., Zhang, X.W. and Kuriyan, J. (2009) Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137, 1293-1307
10. Jeffrey, P.D., Ruso, A.A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J. and Pavletich, N.P. (1995) Mechanism of Cdk activation revealed by the structure of a cyclin A-Cdk2 complex. Nature 376, 313-320
11. Pawson, T. (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203
12. Zhang, W. and Liu, H.T. (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12, 9-18
13. Carpenter, G. (2000) The EGF receptor: a nexus for trafficking and signaling. BioEssays 22, 697-707
14. Garrett, T.P., McKern, N.M., Lou, M., Elleman, T.C., Adams, T.E., Lovrecz, G.O., Zhu, H.J., Walker, F., Frenkel, M.J., Hoyne, P.A. et al. (2002) Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor α. Cell 110, 763-773 (Pubitemid 35283965)
15. Ogiso, H., Ishitani, R., Nureki, O., Fukai, S., Yamanaka, M., Kim, J.H., Saito, K., Sakamoto, A., Inoue, M., Shirouzu, M. and Yokoyama, S. (2002) Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110, 775-787 (Pubitemid 35291060)
16. Ferguson, K.M., Berger, M.B., Mendrola, J.M., Cho, H.S., Leahy, D.J. and Lemmon, M.A. (2003) EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell 11, 507-517 (Pubitemid 36297057)
17. Bouyain, S., Longo, P.A., Li, S., Ferguson, K.M. and Leahy, D.J. (2005) The extracellular region of ErbB4 adopts a tethered conformation in the absence of ligand. Proc. Natl. Acad. Sci. U.S.A. 102, 15024-15029 (Pubitemid 41513328)
18. Hyun-Soo, C. and Leahy, D.J. (2002) Structure of the extracellular region of HER3 reveals an interdomain tether. Science 297, 1330-1333
19. Burgess, A.W., Cho, H.S., Eigenbrot, C., Ferguson, K.M., Garrett, T.P., Leahy, D.J., Lemmon, M.A., Sliwkowski, M.X., Ward, C.W. and Yokoyama, S. (2003) An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12, 541-552 (Pubitemid 37222478)
20. Magun, B.E., Matrisian, L.M. and Bowden, G.T. (1980) Epidermal growth-factor: ability of tumor promoter to alter its degradation, receptor affinity and receptor number. J. Biol. Chem. 255, 6373-6381 (Pubitemid 11229423)
21. Shoyab, M., Delarco, J.E. and Todaro, G.J. (1979) Biologically-active phorbol esters specifically alter affinity of epidermal growth factor membrane receptors. Nature 279, 387-391 (Pubitemid 9184714)
22. Ullrich, A. and Schlessinger, J. (1990) Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212
23. Defize, L.H.K., Boonstra, J., Meisenhelder, J., Kruijer, W., Tertoolen, L.G.J., Tilly, B.C., Hunter, T., Henegouwen, P., Moolenaar, W.H. and Delaat, S.W. (1989) Signal transduction by epidermal growth-factor occurs through the subclass of high-affinity receptors. 109, 2495-2507
24. Friedman, B.A., Frackelton, A.R., Ross, A.H., Connors, J.M., Fujiki, H., Sugimura, T. and Rosner, M.R. (1984) Tumor promoters block tyrosine-specific phosphorylation of the epidermal growth factor receptor. Proc. Natl. Acad. Sci. U.S.A. 81, 3034-3038 (Pubitemid 14109519)
25. Mattoon, D., Klein, P., Lemmon, M.A., Lax, I. and Schlessinger, J. (2004) The tethered configuration of the EGF receptor extracellular domain exerts only a limited control of receptor function. Proc. Natl. Acad. Sci. U.S.A. 101, 923-928 (Pubitemid 38160560)
26. Macdonald, J.L. and Pike, L.J. (2008) Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system. Proc. Natl. Acad. Sci. U.S.A. 105, 112-117
27. Alvarado, D., Klein, D.E. and Lemmon, M.A. (2010) Structural basis for negative cooperativity in growth factor binding to an EGF receptor. Cell 142, 568-579
28. Stryer, L. and Haugland, R.P. (1967) Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. U.S.A. 58, 719-726
29. Carraway, K.L., Koland, J.G. and Cerione, R.A. (1990) Location of the epidermal growth-factor binding-site on the EGF receptor: a resonance energy-transfer study. Biochemistry 29, 8741-8747 (Pubitemid 20302770)
30. Chigaev, A., Buranda, T., Dwyer, D.C., Prossnitz, E.R. and Sklar, L.A. (2003) FRET detection of cellular α4-integrin conformational activation. Biophys. J. 85, 3951-3962 (Pubitemid 37490304)
31. Lehto, M.T. and Sharom, F.J. (2002) Proximity of the protein moiety of a GPI-anchored protein to the membrane surface: a FRET study. Biochemistry 41, 8368-8376 (Pubitemid 34705490)
32. Webb, S.E.D., Roberts, S.K., Needham, S.R., Tynan, C.J., Rolfe, D.J., Winn, M.D., Clarke, D.T., Barraclough, R. and Martin-Fernandez, M.L. (2008) Single-molecule imaging and fluorescence lifetime imaging microscopy show different structures for high- and low-affinity epidermal growth factor receptors in A431 cells. Biophys. J. 94, 808-819
33. Kästner, J., Loeffler, H.H., Roberts, S.K., Martin-Fernandez, M.L. and Winn, M.D. (2009) Ectodomain orientation, conformational plasticity and oligomerization of ErbB1 receptors investigated by molecular dynamics. J. Struct. Biol. 167, 117-128
34. Tynan, C.J., Roberts, S.K., Rolfe, D.J., Clarke, D.T., Loeffler, H.H., Kästner, J., Winn, M.D., Parker, P.J. and Martin-Fernandez, M.L. (2011) Human-EGFR aligned on the plasma membrane adopts key features of Drosophila-EGFR asymmetry. Mol. Cell. Biol. 31, 2241-2252
35. Martin-Fernandez, M., Clarke, D.T., Tobin, M.J., Jones, S.V. and Jones, G.R. (2002) Preformed oligomeric epidermal growth factor receptors undergo an ectodomain structure change during signaling. Biophys. J. 82, 2415-2427 (Pubitemid 34441281)
36. Webb, S.E., Rolfe, D.J., Needham, S.R., Roberts, S.K., Clarke, D.T., McLachlan, C.I., Hobson, M.P. and Martin-Fernandez, M.L. (2008) Simultaneous widefield single molecule orientation and FRET microscopy in cells. Opt. Express 16, 20258-20265
37. Webb, S.E. D., Needham, S.R., Roberts, S.K. and Martin-Fernandez, M.L. (2006) Multidimensional single-molecule imaging in live cells using total-internal-reflection fluorescence microscopy. Opt. Lett. 31, 2157-2159 (Pubitemid 44542716)
38. Wolber, P.K. and Hudson, B.S. (1979) Analytic solution to the Förster energy-transfer problem in two dimensions. Biophys. J. 28, 197-210 (Pubitemid 10196482)
39. van Bueren, J.J.L., Bleeker, W.K., Brannstrom, A., von Euler, A., Jansson, M., Peipp, M., Schneider-Merck, T., Valerius, T., van de Winkel, J.G.J. and Parren, P.W.H.I. (2008) The antibody zalutumumab inhibits epidermal growth factor receptor signaling by limiting intra- and intermolecular flexibility. Proc. Natl. Acad. Sci. U.S.A. 105, 6109-6114 (Pubitemid 351758407)